Localization of functional endothelin receptor signaling complexes in cardiac transverse tubules

J Biol Chem. 2003 Nov 28;278(48):48154-61. doi: 10.1074/jbc.M304396200. Epub 2003 Sep 12.

Abstract

Endothelin-1 (ET-1) is an autocrine factor in the mammalian heart important in enhancing cardiac performance, protecting against myocardial ischemia, and initiating the development of cardiac hypertrophy. The ETA receptor is a seven-transmembrane G-protein-coupled receptor whose precise subcellular localization in cardiac muscle is unknown. Here we used fluorescein ET-1 and 125I-ET-1 to provide evidence for ET-1 receptors in cardiac transverse tubules (T-tubules). Moreover, the ETA receptor and downstream effector phospholipase C-beta 1 were co-localized within T-tubules using standard immunofluorescence techniques, and protein kinase C (PKC)-epsilon-enhanced green fluorescent protein bound reversibly to T-tubules upon activation. Localized photorelease of diacylglycerol further suggested compartmentation of PKC signaling, with release at the myocyte "surface" mimicking the negative inotropic effects of bath-applied PKC activators and "deep" release mimicking the positive inotropic effect of ET-1. The functional significance of T-tubular ET-1 receptors was further tested by rendering the T-tubule lumen inaccessible to bath-applied ET-1. Such "detubulated" cardiac myocytes showed no positive inotropic response to 20 nM ET-1, despite retaining both a nearly normal twitch response to field stimulation and a robust positive inotropic response to 20 nm isoproterenol. We propose that ET-1 enhances myocyte contractility by activating ETA receptor-phospholipase C-beta 1-PKC-epsilon signaling complexes preferentially localized in cardiac T-tubules. Compartmentation of ET-1 signaling complexes may explain the discordant effects of ET-1 versus bath applied PKC activators and may contribute to both the specificity and diversity of the cardiac actions of ET-1.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Blotting, Western
  • Dogs
  • Dose-Response Relationship, Drug
  • Endothelin-1 / metabolism
  • Fluorescein / pharmacology
  • Green Fluorescent Proteins
  • Heart Ventricles / metabolism
  • Isoenzymes / metabolism
  • Isoproterenol / pharmacology
  • Kinetics
  • Luminescent Proteins / metabolism
  • Male
  • Microscopy, Fluorescence
  • Models, Biological
  • Models, Chemical
  • Myocardium / cytology
  • Myocardium / metabolism*
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / physiology*
  • Phospholipase C beta
  • Photons
  • Protein Binding
  • Protein Kinase C / metabolism
  • Protein Kinase C-epsilon
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Endothelin / metabolism*
  • Signal Transduction
  • Type C Phospholipases / metabolism

Substances

  • Endothelin-1
  • Isoenzymes
  • Luminescent Proteins
  • Receptors, Endothelin
  • Green Fluorescent Proteins
  • Prkce protein, rat
  • Protein Kinase C
  • Protein Kinase C-epsilon
  • Type C Phospholipases
  • Phospholipase C beta
  • Isoproterenol
  • Fluorescein